Dataset Information

Multisensory training improves the development of spatial cognition after sight restoration from congenital cataracts.

ABSTRACT: Spatial cognition and mobility are typically impaired in congenitally blind individuals, as vision usually calibrates space perception by providing the most accurate distal spatial cues. We have previously shown that sight restoration from congenital bilateral cataracts guides the development of more accurate space perception, even when cataract removal occurs years after birth. However, late cataract-treated individuals do not usually reach the performance levels of the typically sighted population. Here, we developed a brief multisensory training that associated audiovisual feedback with body movements. Late cataract-treated participants quickly improved their space representation and mobility, performing as well as typically sighted controls in most tasks. Their improvement was comparable with that of a group of blind participants, who underwent training coupling their movements with auditory feedback alone. These findings suggest that spatial cognition can be enhanced by a training program that strengthens the association between bodily movements and their sensory feedback (either auditory or audiovisual).

SUBMITTER: Senna I

PROVIDER: S-EPMC10897914 | biostudies-literature | 2024 Mar

REPOSITORIES: biostudies-literature

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Multisensory training improves the development of spatial cognition after sight restoration from congenital cataracts.

Senna Irene I Piller Sophia S Martolini Chiara C Cocchi Elena E Gori Monica M Ernst Marc O MO

iScience 20240209 3

Spatial cognition and mobility are typically impaired in congenitally blind individuals, as vision usually calibrates space perception by providing the most accurate distal spatial cues. We have previously shown that sight restoration from congenital bilateral cataracts guides the development of more accurate space perception, even when cataract removal occurs years after birth. However, late cataract-treated individuals do not usually reach the performance levels of the typically sighted popula ...[more]

PMID: 38414862

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Project description:Self-motion perception (e.g., when walking/driving) relies on the integration of multiple sensory cues including visual, vestibular, and proprioceptive signals. Changes in the efficacy of multisensory integration have been observed in older adults (OA), which can sometimes lead to errors in perceptual judgments and have been associated with functional declines such as increased falls risk. The objectives of this study were to determine whether passive, visual-vestibular self-motion heading perception could be improved by providing feedback during multisensory training, and whether training-related effects might be more apparent in OAs vs. younger adults (YA). We also investigated the extent to which training might transfer to improved standing-balance. OAs and YAs were passively translated and asked to judge their direction of heading relative to straight-ahead (left/right). Each participant completed three conditions: (1) vestibular-only (passive physical motion in the dark), (2) visual-only (cloud-of-dots display), and (3) bimodal (congruent vestibular and visual stimulation). Measures of heading precision and bias were obtained for each condition. Over the course of 3 days, participants were asked to make bimodal heading judgments and were provided with feedback ("correct"/"incorrect") on 900 training trials. Post-training, participants' biases, and precision in all three sensory conditions (vestibular, visual, bimodal), and their standing-balance performance, were assessed. Results demonstrated improved overall precision (i.e., reduced JNDs) in heading perception after training. Pre- vs. post-training difference scores showed that improvements in JNDs were only found in the visual-only condition. Particularly notable is that 27% of OAs initially could not discriminate their heading at all in the visual-only condition pre-training, but subsequently obtained thresholds in the visual-only condition post-training that were similar to those of the other participants. While OAs seemed to show optimal integration pre- and post-training (i.e., did not show significant differences between predicted and observed JNDs), YAs only showed optimal integration post-training. There were no significant effects of training for bimodal or vestibular-only heading estimates, nor standing-balance performance. These results indicate that it may be possible to improve unimodal (visual) heading perception using a multisensory (visual-vestibular) training paradigm. The results may also help to inform interventions targeting tasks for which effective self-motion perception is important.

Project description:Sensory deprivation prompts extensive structural and functional reorganizations of the cortex resulting in the occupation of space for the lost sense by the intact sensory systems. This process, known as cross-modal plasticity, has been widely studied in individuals with vision or hearing loss. However, little is known on the neuroplastic changes in restoring the deprived sense. Some reports consider the cross-modal functionality maladaptive to the return of the original sense, and others view this as a critical process in maintaining the neurons of the deprived sense active and operational. These controversial views have been challenged in both auditory and vision restoration reports for decades. Recently with the approval of Luxturna as the first retinal gene therapy (GT) drug to reverse blindness, there is a renewed interest for the crucial role of cross-modal plasticity on sight restoration. Employing a battery of task and resting state functional magnetic resonance imaging (rsfMRI), in comparison to a group of sighted controls, we tracked the functional changes in response to auditory and visual stimuli and at rest, in a group of patients with biallelic mutations in the RPE65 gene ("RPE65 patients") before and 3 years after GT. While the sighted controls did not present any evidence for auditory cross-modal plasticity, robust responses to the auditory stimuli were found in occipital cortex of the RPE65 patients overlapping visual responses and significantly elevated 3 years after GT. The rsfMRI results showed significant connectivity between the auditory and visual areas for both groups albeit attenuated in patients at baseline but enhanced 3 years after GT. Taken together, these findings demonstrate that (1) RPE65 patients present with an auditory cross-modal component; (2) visual and non-visual responses of the visual cortex are considerably enhanced after vision restoration; and (3) auditory cross-modal functions did not adversely affect the success of vision restitution. We hypothesize that following GT, to meet the demand for the newly established retinal signals, remaining or dormant visual neurons are revived or unmasked for greater participation. These neurons or a subset of these neurons respond to both the visual and non-visual demands and further strengthen connectivity between the auditory and visual cortices.

Dataset Information

Multisensory training improves the development of spatial cognition after sight restoration from congenital cataracts.

Publications

Multisensory training improves the development of spatial cognition after sight restoration from congenital cataracts.

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